Dynamic branching in a neural network model for probabilistic prediction of sequences.

An important function of the brain is to predict which stimulus is likely to occur based on the perceived cues. The present research studied the branching behavior of a computational network model of populations of excitatory and inhibitory neurons, both analytically and through simulations. Results show how synaptic efficacy, retroactive inhibition and short-term synaptic depression determine the dynamics of selection between different branches predicting sequences of stimuli of different probabilities. Further results show that changes in the probability of the different predictions depend on variations of neuronal gain. Such variations allow the network to optimize the probability of its predictions to changing probabilities of the sequences without changing synaptic efficacy.

Probability, Dependency, and Frequency Are Not All Equally Involved in Statistical Learning.

The ability to learn sequences depends on different factors governing sequence structure, such as transitional probability (TP, probability of a stimulus given a previous stimulus), adjacent or nonadjacent dependency, and frequency. Current evidence indicates that adjacent and nonadjacent pairs are not equally learnable; the same applies to second-order and first-order TPs and to the frequency of the sequences. However, the relative importance of these factors and interactive effects on learning remain poorly understood. The first experiment tested the effects of TPs and dependency separately on the learning of nonlinguistic visual sequences, and the second experiment used the factors of the first experiment and added a frequency factor to test their interactive effects with verbal sequences of stimuli (pseudo-words). The results of both experiments showed higher performance during online learning for first-order TPs in adjacent pairs. Moreover, Experiment 2 indicated poorer performance during offline recall for nonadjacent dependencies and low-frequency sequences. We discuss the results that different factors are not used equally in prediction and memorization.

Learning Higher-Order Transitional Probabilities in Nonhuman Primates.

The extraction of cooccurrences between two events, A and B, is a central learning mechanism shared by all species capable of associative learning. Formally, the cooccurrence of events A and B appearing in a sequence is measured by the transitional probability (TP) between these events, and it corresponds to the probability of the second stimulus given the first (i.e., p(B|A)). In the present study, nonhuman primates (Guinea baboons, Papio papio) were exposed to a serial version of the XOR (i.e., exclusive-OR), in which they had to process sequences of three stimuli: A, B, and C. In this manipulation, first-order TPs (i.e., AB and BC) were uninformative due to their transitional probabilities being equal to .5 (i.e., p(B|A) = p(C|B) = .5), while second-order TPs were fully predictive of the upcoming stimulus (i.e., p(C|AB) = 1). In Experiment 1, we found that baboons were able to learn second-order TPs, while no learning occurred on first-order TPs. In Experiment 2, this pattern of results was replicated, and a final test ruled out an alternative interpretation in terms of proximity to the reward. These results indicate that a nonhuman primate species can learn a nonlinearly separable problem such as the XOR. They also provide fine-grained empirical data to test models of statistical learning on the interaction between the learning of different orders of TPs. Recent bioinspired models of associative learning are also introduced as promising alternatives to the modeling of statistical learning mechanisms.

Determinants of multiple semantic priming: a meta-analysis and spike frequency adaptive model of a cortical network.

Recall and language comprehension while processing sequences of words involves multiple semantic priming between several related and/or unrelated words. Accounting for multiple and interacting priming effects in terms of underlying neuronal structure and dynamics is a challenge for current models of semantic priming. Further elaboration of current models requires a quantifiable and reliable account of the simplest case of multiple priming resulting from two primes on a target. The meta-analytic approach offers a better understanding of the experimental data from studies on multiple priming regarding the additivity pattern of priming. The meta-analysis points to the effects of prime-target stimuli onset asynchronies on the pattern of underadditivity, overadditivity, or strict additivity of converging activation from multiple primes. The modeling approach is then constrained by results of the meta-analysis. We propose a model of a cortical network embedding spike frequency adaptation, which allows frequency and time-dependent modulation of neural activity. Model results give a comprehensive understanding of the meta-analysis results in terms of dynamics of neuron populations. They also give predictions regarding how stimuli intensities, association strength, and spike frequency adaptation influence multiple priming effects.

Statistical learning of unbalanced exclusive-or temporal sequences in humans.

A pervasive issue in statistical learning has been to determine the parameters of regularity extraction. Our hypothesis was that the extraction of transitional probabilities can prevail over frequency if the task involves prediction. Participants were exposed to four repeated sequences of three stimuli (XYZ) with each stimulus corresponding to the position of a red dot on a touch screen that participants were required to touch sequentially. The temporal and spatial structure of the positions corresponded to a serial version of the exclusive-or (XOR) that allowed testing of the respective effect of frequency and first- and second-order transitional probabilities. The XOR allowed the first-order transitional probability to vary while being not completely related to frequency and to vary while the second-order transitional probability was fixed (p(Z|X, Y) = 1). The findings show that first-order transitional probability prevails over frequency to predict the second stimulus from the first and that it also influences the prediction of the third item despite the presence of second-order transitional probability that could have offered a certain prediction of the third item. These results are particularly informative in light of statistical learning models.

Benefits and pitfalls of data compression in visual working memory.

Data compression in memory is a cognitive process allowing participants to cope with complexity to reduce information load. However, previous studies have not yet considered the hypothesis that this process could also lead to over-simplifying information due to haphazard amplification of the compression process itself. For instance, we could expect that the over-regularized features of a visual scene could produce false recognition of patterns, not because of storage capacity limits but because of an errant compression process. To prompt memory compression in our participants, we used multielement visual displays for which the underlying information varied in compressibility. The compressibility of our material could vary depending on the number of common features between the multi-dimensional objects in the displays. We measured both accuracy and response times by probing memory representations with probes that we hypothesized could modify the participants' representations. We confirm that more compressible information facilitates performance, but a more novel finding is that compression can produce both typical memory errors and lengthened response times. Our findings provide clearer evidence of the forms of compression that participants carry out.

Neuronal mechanisms for sequential activation of memory items: Dynamics and reliability.

In this article we present a biologically inspired model of activation of memory items in a sequence. Our model produces two types of sequences, corresponding to two different types of cerebral functions: activation of regular or irregular sequences. The switch between the two types of activation occurs through the modulation of biological parameters, without altering the connectivity matrix. Some of the parameters included in our model are neuronal gain, strength of inhibition, synaptic depression and noise. We investigate how these parameters enable the existence of sequences and influence the type of sequences observed. In particular we show that synaptic depression and noise drive the transitions from one memory item to the next and neuronal gain controls the switching between regular and irregular (random) activation.

Linguistic processes do not beat visuo-motor constraints, but they modulate where the eyes move regardless of word boundaries: Evidence against top-down word-based eye-movement control during reading.

Where readers move their eyes, while proceeding forward along lines of text, has long been assumed to be determined in a top-down word-based manner. According to this classical view, readers of alphabetic languages would invariably program their saccades towards the center of peripheral target words, as selected based on the (expected) needs of ongoing (word-identification) processing, and the variability in within-word landing positions would exclusively result from systematic and random errors. Here we put this predominant hypothesis to a strong test by estimating the respective influences of language-related variables (word frequency and word predictability) and lower-level visuo-motor factors (word length and saccadic launch-site distance to the beginning of words) on both word-skipping likelihood and within-word landing positions. Our eye-movement data were collected while forty participants read 316 pairs of sentences, that differed only by one word, the prime; this was either semantically related or unrelated to a following test word of variable frequency and length. We found that low-level visuo-motor variables largely predominated in determining which word would be fixated next, and where in a word the eye would land. In comparison, language-related variables only had tiny influences. Yet, linguistic variables affected both the likelihood of word skipping and within-word initial landing positions, all depending on the words' length and how far on average the eye landed from the word boundaries, but pending the word could benefit from peripheral preview. These findings provide a strong case against the predominant word-based account of eye-movement guidance during reading, by showing that saccades are primarily driven by low-level visuo-motor processes, regardless of word boundaries, while being overall subject to subtle, one-off, language-based modulations. Our results also suggest that overall distributions of saccades' landing positions, instead of truncated within-word landing-site distributions, should be used for a better understanding of eye-movement guidance during reading.

Dopaminergic neuromodulation of semantic priming in a cortical network model.

Semantic priming between items stored and associated in memory underlies contextual recall. Response times to process a given target item are shorter when following presentation of a related prime item than when it is unrelated. The study of priming effects allows investigating the structure of semantic networks as a function of association strength and number of links relating the prime and target. Behavioral data from divided visual field experiments in healthy subjects show a variability in the magnitude of priming effects when the left or right hemisphere is primary involved. Data from schizophrenic patients also exhibit variability in priming magnitude compared to data from healthy subjects. Mathematical models of cortical networks allow theorists to understand the link between the physiology of single neurons and synapses and network behavior. Computational modelling can replicate electrophysiological recordings of cortical neurons in monkeys, that exhibit two types of task-related activity, 'retrospective' (related to a previously shown stimulus) and 'prospective' (related to a stimulus expected to appear, due to learned association between both stimuli). Experimental studies of associative priming report priming effects on behavioral data in both human and monkeys. Cortical network models can account for a large variety of priming effects observed in human, and for the dependence of retrospective activity on dopamine neuromodulation. Here, we investigate how variable levels of dopamine in a model of a cortical network can modulate prospective activity to vary the magnitude of semantic priming. We simulate a biologically realistic network of integrate and fire neurons to study the effects of dopaminergic neuromodulation of NMDA receptors of glutamatergic and gabaergic neurons on semantic priming dynamics. Results support the possibility that different levels of dopaminergic neuromodulation can subtend hemispheric differences in semantic priming, corresponding to focused priming in the left hemisphere and to extended priming in the right hemisphere. Furthermore, results can account for priming perturbations in schizophrenia depending on the level of dopamine.

Latching dynamics in neural networks with synaptic depression.

Prediction is the ability of the brain to quickly activate a target concept in response to a related stimulus (prime). Experiments point to the existence of an overlap between the populations of the neurons coding for different stimuli, and other experiments show that prime-target relations arise in the process of long term memory formation. The classical modelling paradigm is that long term memories correspond to stable steady states of a Hopfield network with Hebbian connectivity. Experiments show that short term synaptic depression plays an important role in the processing of memories. This leads naturally to a computational model of priming, called latching dynamics; a stable state (prime) can become unstable and the system may converge to another transiently stable steady state (target). Hopfield network models of latching dynamics have been studied by means of numerical simulation, however the conditions for the existence of this dynamics have not been elucidated. In this work we use a combination of analytic and numerical approaches to confirm that latching dynamics can exist in the context of a symmetric Hebbian learning rule, however lacks robustness and imposes a number of biologically unrealistic restrictions on the model. In particular our work shows that the symmetry of the Hebbian rule is not an obstruction to the existence of latching dynamics, however fine tuning of the parameters of the model is needed.

Semantic integration by pattern priming: experiment and cortical network model.

Neural network models describe semantic priming effects by way of mechanisms of activation of neurons coding for words that rely strongly on synaptic efficacies between pairs of neurons. Biologically inspired Hebbian learning defines efficacy values as a function of the activity of pre- and post-synaptic neurons only. It generates only pair associations between words in the semantic network. However, the statistical analysis of large text databases points to the frequent occurrence not only of pairs of words (e.g., "the way") but also of patterns of more than two words (e.g., "by the way"). The learning of these frequent patterns of words is not reducible to associations between pairs of words but must take into account the higher level of coding of three-word patterns. The processing and learning of pattern of words challenges classical Hebbian learning algorithms used in biologically inspired models of priming. The aim of the present study was to test the effects of patterns on the semantic processing of words and to investigate how an inter-synaptic learning algorithm succeeds at reproducing the experimental data. The experiment manipulates the frequency of occurrence of patterns of three words in a multiple-paradigm protocol. Results show for the first time that target words benefit more priming when embedded in a pattern with the two primes than when only associated with each prime in pairs. A biologically inspired inter-synaptic learning algorithm is tested that potentiates synapses as a function of the activation of more than two pre- and post-synaptic neurons. Simulations show that the network can learn patterns of three words to reproduce the experimental results.

Eye movements in reading isolated words: evidence for strong biases towards the center of the screen.

Three experiments were conducted that compared the eye movement pattern to a peripheral word or letter string as a function of the position of an initial fixation stimulus relative to the center of the screen and the straight-ahead position. Results revealed a strong bias of the eye behavior towards the center of the screen, but not towards the straight-ahead position. Saccades were greater in length, and landed closer to the center of words/strings when launched from a position left of center than when launched from either center or right part of the screen. In addition, the initial saccade launch site was deviated to the right, or to the left of the initial fixation stimulus depending on where relative to the center of the screen the fixation stimulus was displayed. Data were interpreted with the assumption that saccades are programmed in a visual reference framework, with saccade amplitude being computed in relative coordinates. Further research will determine whether the observed bias generalizes to text reading.

Inter-synaptic learning of combination rules in a cortical network model.

Selecting responses in working memory while processing combinations of stimuli depends strongly on their relations stored in long-term memory. However, the learning of XOR-like combinations of stimuli and responses according to complex rules raises the issue of the non-linear separability of the responses within the space of stimuli. One proposed solution is to add neurons that perform a stage of non-linear processing between the stimuli and responses, at the cost of increasing the network size. Based on the non-linear integration of synaptic inputs within dendritic compartments, we propose here an inter-synaptic (IS) learning algorithm that determines the probability of potentiating/depressing each synapse as a function of the co-activity of the other synapses within the same dendrite. The IS learning is effective with random connectivity and without either a priori wiring or additional neurons. Our results show that IS learning generates efficacy values that are sufficient for the processing of XOR-like combinations, on the basis of the sole correlational structure of the stimuli and responses. We analyze the types of dendrites involved in terms of the number of synapses from pre-synaptic neurons coding for the stimuli and responses. The synaptic efficacy values obtained show that different dendrites specialize in the detection of different combinations of stimuli. The resulting behavior of the cortical network model is analyzed as a function of inter-synaptic vs. Hebbian learning. Combinatorial priming effects show that the retrospective activity of neurons coding for the stimuli trigger XOR-like combination-selective prospective activity of neurons coding for the expected response. The synergistic effects of inter-synaptic learning and of mixed-coding neurons are simulated. The results show that, although each mechanism is sufficient by itself, their combined effects improve the performance of the network.

Early dynamics of the semantic priming shift.

Semantic processing of sequences of words requires the cognitive system to keep several word meanings simultaneously activated in working memory with limited capacity. The real- time updating of the sequence of word meanings relies on dynamic changes in the associates to the words that are activated. Protocols involving two sequential primes report a semantic priming shift from larger priming of associates to the first prime to larger priming of associates to the second prime, in a range of long SOAs (stimulus-onset asynchronies) between the second prime and the target. However, the possibility for an early semantic priming shift is still to be tested, and its dynamics as a function of association strength remain unknown. Three multiple priming experiments are proposed that cross-manipulate association strength between each of two successive primes and a target, for different values of short SOAs and prime durations. Results show an early priming shift ranging from priming of associates to the first prime only to priming of strong associates to the first prime and all of the associates to the second prime. We investigated the neural basis of the early priming shift by using a network model of spike frequency adaptive cortical neurons (e.g., Deco & Rolls, 2005), able to code different association strengths between the primes and the target. The cortical network model provides a description of the early dynamics of the priming shift in terms of pro-active and retro-active interferences within populations of excitatory neurons regulated by fast and unselective inhibitory feedback.

Dynamics of the semantic priming shift: behavioral experiments and cortical network model.

Multiple semantic priming processes between several related and/or unrelated words are at work during the processing of sequences of words. Multiple priming generates rich dynamics of effects depending on the relationship between the target word and the first and/or second prime previously presented. The experimental literature suggests that during the on-line processing of the primes, the activation can shift from associates to the first prime to associates to the second prime. Though the semantic priming shift is central to the on-line and rapid updating of word meanings in the working memory, its precise dynamics are still poorly understood and it is still a challenge to model how it functions in the cerebral cortex. Four multiple priming experiments are proposed that cross-manipulate delays and association strength between the primes and the target. Results show for the first time that association strength determines complex dynamics of the semantic priming shift, ranging from an absence of a shift to a complete shift. A cortical network model of spike frequency adaptive neuron populations is proposed to account for the non-continuous evolution of the priming shift over time. It allows linking the dynamics of the priming shift assessed at the behavioral level to the non-linear dynamics of the firing rates of neurons populations.

Semantic priming in a cortical network model.

Contextual recall in humans relies on the semantic relationships between items stored in memory. These relationships can be probed by priming experiments. Such experiments have revealed a rich phenomenology on how reaction times depend on various factors such as strength and nature of associations, time intervals between stimulus presentations, and so forth. Experimental protocols on humans present striking similarities with pair association task experiments in monkeys. Electrophysiological recordings of cortical neurons in such tasks have found two types of task-related activity, "retrospective" (related to a previously shown stimulus), and "prospective" (related to a stimulus that the monkey expects to appear, due to learned association between both stimuli). Mathematical models of cortical networks allow theorists to understand the link between the physiology of single neurons and synapses, and network behavior giving rise to retrospective and/or prospective activity. Here, we show that this type of network model can account for a large variety of priming effects. Furthermore, the model allows us to interpret semantic priming differences between the two hemispheres as depending on a single association strength parameter.